Relations of phototrophic bacteria and the evolution of photosynthesis

I am very interested in the evolution of photosynthesis. From my research, I have come to conclude that photosynthesis evolved near the root or at the root of the tree of life of the domain Bacteria. In other words, the core components of photosynthesis such as reaction center proteins or the enzymatic components of the chlorophyll and bacteriochlorophyll synthesis pathway, originated before most of the known phyla of bacteria appeared for the first time.

A way to understand how and when photosynthesis originated we need to understand the phylogenetic relations of bacteria. Known phototrophic bacteria are found in seven phyla of bacteria: Cyanobacteria, Firmicutes, Chloroflexi, Chlorobi, Proteobacteria, Acidobacteria, and Gemmatimonadetes. In addition to this, it has been shown that the phylum Actinobacteria might have been ancestrally capable of phototrophy, because some of the strains in this phylum seem to have a vestigial chlorophyll synthesis pathway.

An interesting aspect about the evolution of photosynthesis is that all the phyla containing phototrophic bacteria are clustered within non-phototrophic groups.

Within the phylum Chlorobi there are at least two classes, Chlorobea and Ignavibacteria. All described members of the Ignavibacteria class lack phototrophy. The phylum Chlorobi is very closely related to the phylum Bacteroidetes and no phototrophic Bacteroidetes have been described yet.

Within the phylum Firmicutes, phototrophy is only found in the family Heliobacteraceae (Heliobacteria). Heliobacteria is closely related to the family Peptococcaceae, with the closest strains to Heliobacterium modesticaldum (the only fully sequenced strain of Heliobacteria) being Desulfitobacterium and Synthrophobotulus, which are not phototrophic. What is more, the phylum Firmicutes is subdivided in several classes including, Clostridia, Bacilli, and others. The Heliobacteraceae family belongs to the class Clostridia.

Within the phylum Proteobacteria, only the Alpha-, Beta-, and Gammaproteobacteria are phototrophic, but this is not a universal trait among them. There are many representative of these classes that are not phototrophic. Currently there are no described strains in the class Delta- and Epsilonproteobacteria  with phototrophy.

Only a single strain in the phylum Acidobacteria has been described with phototrophy. Chloracidobacterium thermophilum, but it is probably not the only one. All other strains described in this phylum are non-phototrophic. It should be said though, that only very few strains in this phylum have been characterized. Acidobacteria is closely related to the Proteobacteria as demonstrated by many phylogenomic analysis, sometimes the phylum actually clusters within the Deltaproteobacteria. It is very likely that Acidobacteria and Proteobacteria shared a common ancestor.

Cyanobacteria were thought to be made of only phototrophic strains, however the discovery of Melainabacteria has shown that also Cyanobacteria have very close non-phototrophic relatives. It has been suggested that Melainabacteria should be classified within the phylum Cyanobacteria, and the known photosynthetic Cyanobacteria should be downgraded to class level.

The phylum Chloroflexi is made of about eight different classes, only two of them, the Chloroflexia and the Anaerolineae, have been shown to contain phototrophic strains.

Only one strain in the phylum Gemmatimonadetes has been described to be capable of phototrophy. It appears that this strain obtained photosynthesis via horizontal gene transfer from proteobacteria. However, metagenomic analysis has demonstrated that there are more strains in this phylum with phototrophy.

It is usually considered that the scattered distribution of phototrophy in the tree of life of bacteria is the outcome of horizontal gene transfer, but this is probably not completely correct. So it is suggested for example, that phototrophy could have evolved in the phylum Chlorobi and then via horizontal gene transfer it seeded all other branches. In the case of Cyanobacteria, it is common to suggest that the phylum obtained both reaction centers from two distinct phyla of anoxygenic phototrophic bacteria. This is just one example but almost all possible origins have been considered, including Heliobcteria, Chloroflexi, Cyanobacteria, and Proteobacteria as the original innovators of photosynthesis.

There is absolutely no data or piece of evidence to suggest that photosynthesis originated in any of the described phototrophic groups. All reaction center proteins and all core proteins of the chlorophyll synthesis pathway (e.g. Mg-chelatase, Mg-protoporphyrin IX methyl transferase, protochlorophyllide a oxidoredutase, chlorophyllide a oxidoreductase) share a common origin. They should have descended from ancestral forms that existed more than 3.5 billion years ago. Therefore these ancestral forms should have existed before they diversified into the forms commonly found in the extant groups that we have right now. None of the groups of phototrophs we know today carry these ancestral forms of reaction center proteins or chlorophyll synthesis genes. So for example, suggesting that photosynthesis evolved in the Chlorobi implies that the phylum Chlorobi already existed 3.5 billion years ago; not only that, but it implies that the divergence of Ignavibacteria and Chlorbia had already occurred then, and the divergence of Bacteroidetes and Chlorbi too, and in consequence it has the ultimate implication that the vast majority of groups of bacteria had already differentiated at that time: which is virtually impossible. The same applies if we select any of the phototrophic groups as possible birth places of photosynthesis. In fact, it is very likely that the divergence events that caused the diversification of the group of bacteria mentioned above: Chlorobi/Bacteroidetes, Cyanobacteria/Melainabacteria, Acidobacteria/Proteobacteria, Chlostridia/Bacilli occurred around the Great Oxygenation Event or after. Most likely, photosynthesis is an ancestral trait of the domain Bacteria that has been lost as the different groups of microbes adapted to an oxygenic world, to heterotrophic lifestyles (due to global primary production being relegated to oxygenic photosynthesis), and to live in symbiotic or parasitic relationships with all eukaryotes on Earth. This is valid even if horizontal gene transfer has occurred among ancestor of today’s phyla at some point in time. The only convincing and unambiguous case of horizontal gene transfer of phototrophy is the case of Gemmatimonas and this probably occurred only recently.